Effects of temperature and habitat complexity on an urban tree pest (Tinocallis kahawaluokalani), natural enemies, and predation services in the city

  • Sarah E. ParsonsEmail author
  • Kyle S. Sozanski
  • Alyanna A. Wilson
  • Steven D. Frank


Trees provide many ecosystem services in our urban environments. However, city trees are often stressed by pests and hot urban temperatures. Our research highlights how temperature affects a common tree pest, crape myrtle aphid (Tinocallis kahawaluokalani), natural enemies, and egg predation services on crape myrtles in the city. This research addresses an area of study that has largely been unexplored, effects of temperature on urban natural enemies, and it sheds light on how hot urban temperatures affect one species of piercing-sucking herbivore, a guild that is generally thought to be benefitted in hot city environments. To test our hypothesis that temperature increases T. kahawaluokalani density, fecundity and population growth, yet decreases natural enemy density and egg predation services on street trees, we collected data on crape myrtle trees in Raleigh, NC and conducted lab experiments in 2018. We collected canopy temperature and arthropod data on study trees from May–August and measured local structural complexity around trees and plant water potential. Aphid density decreased with hotter urban temperatures. However, natural enemies and egg predation were not affected by temperature. Natural enemy density was most correlated with local structural complexity. Together these findings suggest that increasing local structural complexity around trees may be a way to support natural enemies on both cool and hot urban trees. Our findings also emphasize the need for similar studies that evaluate temperature effects on common tree pests to help landscape managers prioritize pest targets for pest control in a warmer and more urban world.


Biological control Aphids Natural enemies Urban trees Urban heat island 



We thank Tom Wentworth, George Hess, and Michael Reiskind, who provided helpful advice along the way. We also thank Elsa Youngsteadt, Emily Griffith, and Michael Just for statistical guidance and feedback. We thank Matt Bertone, who provided helpful identification advice, as well as Annemarie Nagle, Leo Kerner, Cat Crofton, Ian McAreavy, Danielle Schmidt, Nicole Bissonnette, Aimee Dalsimer, Janis Arrojado, Kelly Harris, Logan Tyson, Doua Jim Lor, Tommy Pleasant, Anna Holmquist and all of the dedicated lab members who helped collect and analyze data for this project. This project was supported by Cooperative Agreement no. G15AP00153 from the United States Geological Survey to S.D.F. Its contents are solely the responsibility of the authors and do not necessarily represent the views of the Department of the Interior Southeast Climate Adaptation Science Center or the USGS. Funding for this work was also provided by U.S. Department of Agriculture, Grant Award Number: 2013-02476 to S.D.F. and the Southeast Climate Adaptation Science Center graduate fellowship awarded to S.E.P. The North Carolina State University Department of Entomology also contributed support for this research. North Carolina School of Science and Mathematics also contributed support for this research.

Author’s contributions

S.E.P and S.D.F conceived of experimental design. S.E.P. collected and analyzed the data. K.S.S. and A.A.W. collected data for lab experiments. All authors contributed to drafts and gave approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11252_2019_900_MOESM1_ESM.docx (1.9 mb)
ESM 1 (DOCX 1926 kb)


  1. Alverson DR, Allen RK (1991) Life history of crapemyrtle aphid. Southern Nursery Association Research Conference 36:164–170Google Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. CrossRefGoogle Scholar
  3. Bennett AB, Gratton C (2012) Measuring natural pest suppression at different spatial scales affects the importance of local variables. Environ Entomol 41(5):1077–1085CrossRefGoogle Scholar
  4. Brightwell RJ, Silverman J (2011) The argentine ant persists through unfavorable winters via a mutualism facilitated by a native tree. Environ Entomol 40(5):1019–1026CrossRefGoogle Scholar
  5. Burkman CE, Gardiner MM (2014) Urban greenspace composition and landscape context influence natural enemy community composition and function. Biol Control 75:58–67CrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, Fort Collins (CO)Google Scholar
  7. Chappell MR, Braman SK, Williams-Woodward J, Knox GW (2012) Optimizing plant health and pest management of Lagerstroemia spp. in commercial production on and landscape situations in the southeastern United States: a review. J Environ Hortic 30:161–172Google Scholar
  8. Dale AG, Frank SD (2014) Urban warming trumps natural enemy regulation of herbivorous pests. Ecol Appl 24(7):1596–1607CrossRefGoogle Scholar
  9. Dale AG, Frank SD (2017) Warming and drought combine to increase pest insect fitness on urban trees. PLoS One 12(3):e0173844. CrossRefGoogle Scholar
  10. Dale AG, Youngsteadt E, Frank SD (2016) Forecasting the effects of heat and pests on urban trees: impervious surface thresholds and the ‘pace-to-plant’ technique. Arboric. & Urb. Forestry. 42(3):181–191Google Scholar
  11. Davies FT, Castro-Jimenez Y (1989) Water relations of Lagerstroemia indica grown in amended media under drought stress. Sci Hortic 41(1):97–104CrossRefGoogle Scholar
  12. Dozier HL (1926) Crepe myrtle plant louse. J. Economic. Entomology 19:800Google Scholar
  13. Dreistadt SH, Dahlsten DL, Frankie GW (1990) Urban forests and insect ecology. BioSci. 40(3):192–198CrossRefGoogle Scholar
  14. Egerer M, Li K, Ong T (2018) Context matters: contrasting ladybird beetle responses to urban environments across two US regions. Sustainability. 10(6):1829CrossRefGoogle Scholar
  15. Faeth SH, Bang C, Saari S (2011) Urban biodiversity: patterns and mechanisms. Ann N Y Acad Sci 1223:69–81CrossRefGoogle Scholar
  16. Frank SD (2019) A survey of key arthropod pests on common southeastern street trees. Arboricult Urban For 45(5):155–166Google Scholar
  17. Gardiner MM, Prajzner SP, Burkman CE, Albro S, Grewal PS (2014) Vacant land conversion to community gardens: influences on generalist arthropod predators and biocontrol services in urban greenspaces. Urban Ecosyst 17:101–122CrossRefGoogle Scholar
  18. Hamblin AL, Youngsteadt E, Lopez-Uribe MM, Frank SD (2017) Physiological thermal limits predict differential responses of bees to urban heat-island effects. Biol Lett 13:20170125CrossRefGoogle Scholar
  19. Hanks LM, Denno RF (1993) Natural enemies and plant water relations influence the distribution of an armored scale insect. Ecology. 74(4):1081–1091CrossRefGoogle Scholar
  20. Hartig F. (2019) DHARMa: Residual diagnostics for hierarchical (Multi-Level/Mixed) Regression Models. R Package version 0.2.4.
  21. Herbert JJ. (2009) Multitritrophic interactions among crape myrtles Lagerstroemia spp., crape myrtle aphids Sarucallis kahawaluokalani and aphid predators. University of Florida. PhD DissertationGoogle Scholar
  22. Herbert JJ, Mizel RF, Mcauslan HJ (2009) Host preference of the crape myrtle aphid (Hemiptera: Aphididae) and host suitability of crape myrtle cultivars. Environ Entomol 38(4):1155–1160CrossRefGoogle Scholar
  23. Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology. 85(5):1383–1398CrossRefGoogle Scholar
  24. Kim HH (1992) Urban heat island. Int J Remote Sens 13:2319–2336CrossRefGoogle Scholar
  25. Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43:195–216CrossRefGoogle Scholar
  26. Kropczynska D, Vrie M, Tomczyk A (1988) Bionomics of Eotetranychus tiliarium and its Phytoseiid predators. Exp Appl Acarol 5(1):65–81CrossRefGoogle Scholar
  27. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45(1):175–201CrossRefGoogle Scholar
  28. Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex structured habitats: a meta-analytical synthesis. Oecologia. 139(1):1–10CrossRefGoogle Scholar
  29. Lefcheck JS (2015) piecewiseSEM: piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol 7(5):573–579CrossRefGoogle Scholar
  30. Letourneau DK (1987) The enemies hypothesis: Tritrophic interactions and vegetation diversity in tropical agroecosystems. Ecology 68(6):1616–1622CrossRefGoogle Scholar
  31. Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutierrez C, Lopez SD, Majia JL et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21(1):9–21CrossRefGoogle Scholar
  32. Levinsson A, Konijnendijk van den Bosch C, Oxell C, Fransson AM (2015) Visual assessments of establishment success in urban Prunus avium and Quercus rubra in relation to water status and crown morphological characteristics. Urban For Urban Green 14(218):224Google Scholar
  33. Long LC, D’Amico V, Frank SD (2019) Urban forest fragments buffer trees from warming and pests. Sci Total Environ 658:1523–1530CrossRefGoogle Scholar
  34. Lowenstein DM, Minor ES (2018) Herbivores and natural enemies of Brassica crops in urban agriculture. Urban Ecosyst 21:519–529CrossRefGoogle Scholar
  35. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176CrossRefGoogle Scholar
  36. Meineke EK, Frank SD (2018) Water availability drives urban tree growth responses to herbivory and warming. J Appl Ecol:1–13Google Scholar
  37. Meineke EK, Dunn RR, Sexton JO, Frank SD (2013) Urban warming drives insect pest abundance on street trees. PLoS One 1, 8(3)Google Scholar
  38. Meineke EK, Dunn RR, Frank SD (2014) Early pest development and loss of biological control are associated with urban warming. Biol Lett 10(11):20140586CrossRefGoogle Scholar
  39. Meineke EK, Youngsteadt E, Dunn RR, Frank SD (2016) Urban warming reduces aboveground carbon storage. Proc R Soc B 283:20161574CrossRefGoogle Scholar
  40. Meineke EK, Holmquist AJ, Wimp GM, Frank SD (2017) Changes in spider community composition are associated with urban temperature, not herbivore abundance. J Urban Econ 3(1)Google Scholar
  41. Mizell RF (2007) Impact of Harmonia axyridis (Coleoptera: Coccinellidae) on native arthropod predators in pecan and crape myrtle. Fla Entomol 90:524–536CrossRefGoogle Scholar
  42. Mizell RF, Knox GW (1993) Susceptibility of crape myrtle, Lagerstroemia indica, to the Crapemyrtle aphid (Homoptera: Aphididae) in North Florida. J Entomol Sci 28(1):7CrossRefGoogle Scholar
  43. Mizell RF, Schifauer DE (1987) Seasonal abundance of the crapemyrtle aphid Sarucallis kahawaluokalani (Kirkaldy) in relation to the pecan aphids Monellia caryella (Fitch) and Monelliopsis pecanis (Bissell) and their common predators. Entomophaga 32:511–520CrossRefGoogle Scholar
  44. Mizell RF, Benne FD, Reed DK (2002) Unsuccessful search for parasites of the crapemyrtle aphid, Tinocallis kahawaluokalani (Homoptera: Aphididae). Fla Entomol 85:521–523CrossRefGoogle Scholar
  45. NOAA. (n.d.) National Weather Service Forecast Office. Raleigh NC Normal Daily NC Maximum Temperatures. Accessed 10 January 2019
  46. Nowak DJ, Dwyer JF (2000) Understanding the costs and benefits of urban forest ecosystems in J.E. Kuser, editor. Handbook of community and urban forestry in the Northeast. Kluwer, New YorkGoogle Scholar
  47. Nuessly GS, Sterling WL (1994) Mortality of Helicoverpa zea eggs in cotton as a function of oviposition sites, predator species, and desiccation. Pop Ecol 23(5)Google Scholar
  48. Parsons SE, Frank SD (2019) Urban tree pests and natural enemies respond to habitat at different spatial scales. J Urban Econ 5(1):1–15Google Scholar
  49. Pfannenstiel RS, Yeargan KV (2002) Identification and diel activity patterns of predators attacking Helicoverpa zea eggs in soybean and sweet corn. Environ Entomol 31(2):232–241CrossRefGoogle Scholar
  50. Philpott SM, Bichier P (2017) Local and landscape drivers of predation services in urban gardens. Ecol Appl 27(3):966–976CrossRefGoogle Scholar
  51. Pimental D (1961) The influence of plant spatial patterns on insect populations. Ann Entomol Soc Am 54:61–69CrossRefGoogle Scholar
  52. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL Accessed Apr 2019
  53. Raupp MJ, Koehler CS, Davidson JA (1992) Advances in implementing integrated pest management for woody landscape plants. Annu Rev Entomol 37:561–585CrossRefGoogle Scholar
  54. Raupp MJ, Shrewsbury PM, Herms DA (2010) Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol 55(1):19–38CrossRefGoogle Scholar
  55. Raupp MJ, Shrewsbury PM, Herms DA (2012) Diasters by design: outbreaks along urban gradients. In: Barbosa P, Letourneau DK, Agrawal AA (eds) Insect outbreaks revisited. First Edition. Blackwell Publishing, Hoboken, pp 314–333Google Scholar
  56. Riddle TC, Mizell RF (2016) Use of crape myrtle, Lagerstroemia (Myrtales: Lythraceae), cultivars as a pollen source by native and non-native bees in Quincy, FL. Fla Entomol 99(1):38–46CrossRefGoogle Scholar
  57. Rocha EA, Souza ENF, Bleakley LAD, Burley C, Mott JL, Rue-Glutting G, Fellowes MDE (2018) Influence of urbanisation and plants on the diversity and abundance of aphids and their ladybird and hoverfly predators in domestic gardens. Eur J Entomol 115:140–149CrossRefGoogle Scholar
  58. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica: Oleracea). Ecol Monogr 43(1):95–124CrossRefGoogle Scholar
  59. Santesteban LG, Miranda C, Royo JB (2010) Suitability of pre-dawn and stem water potential as indicators of vineyard water status in cv. Tempranillo. Aust J Grape Wine Res 17:43–51CrossRefGoogle Scholar
  60. Sattler T, Duelli P, Obrist M, Arlettaz R, Moretti M (2010) Response of arthropod species richness and functional groups to urban habitat structure and management. Landsc Ecol 25(6):941–954CrossRefGoogle Scholar
  61. Savi T, Bertuzzi S, Branca S, Tretiach M, Nardini A (2015) Drought-induced xylem cavitation and hydraulic deterioration: risk factors for urban trees under climate change? New Phytol 205:1106–1116CrossRefGoogle Scholar
  62. Schneider K, Balder H, Jackel B, Pradel B (2000) Bionomics of Eotetranychus tiliarum as influenced by key factors. International symposium, plant health in urban horticulture; Brunswick. Germany. 370:102–108Google Scholar
  63. Shrewsbury PM, Raupp MJ (2000) Evaluation of components of vegetational texture for predicting azalea lace bug, Stephanitis pyrioides (Heteroptera: Tingidae), abundance in managed landscapes. Environ Entomol 29(5):919–926CrossRefGoogle Scholar
  64. Shrewsbury PM, Raupp MJ (2006) Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes? Ecol Appl 16(1):262–272CrossRefGoogle Scholar
  65. Tooker JF, Hanks LM (2000) Influence of plant community structure on natural enemies of pine needle scale (Homoptera: Diaspididae) in urban landscapes. Environ Entomol 29(6):1305 11CrossRefGoogle Scholar
  66. Way MJ, Cammell ME, Paiva MR (1992) Studies on egg predation by ants especially on the eucalyptus borer Phoracantha semipunctata in Portugal. Bull Entomol Res 82(3):425 432CrossRefGoogle Scholar
  67. Youngsteadt E, Ernst AF, Dunn RR, Frank SD (2016) Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands. Glob Chang Biol 23:1436–1447. CrossRefGoogle Scholar
  68. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New YorkCrossRefGoogle Scholar
  69. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common Statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar
  70. Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Glob Chang Biol 12:27 41CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Entomology & Plant PathologyNorth Carolina State UniversityRaleighUSA
  2. 2.North Carolina School of Science and MathDurhamUSA

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